Journal of Pharmaceutical Research International

32(11): 84-92, 2020; Article no.JPRI.58935 ISSN: 2456-9119 (Past name: British Journal of Pharmaceutical Research, Past ISSN: 2231-2919, NLM ID: 101631759)

Medicinal , Anoectochilus: Distribution, Ecology, Commercial Value and Use in North Vietnam

Trinh Ngoc Bon1, Trieu Thai Hung1, Phung Dinh Trung1, Tran Cao Nguyen1, Dang Thi Hai Ha1, Nguyen Thi Hoai Anh1, Hoang Thanh Son1, Tran Hai Long1, Pham Quang Tuyen1, Ninh Viet Khuong1, Tran Hoang Quy1, Vu Van Nam2 and Tran Van Do1*

1Silviculture Research Institute, Vietnamese Academy of Forest Sciences, Hanoi, Vietnam. 2Department of Lai Chau Forest Protection, Dong Phong Ward, Lai Chau City, Lai Chau Province, Vietnam.

Authors’ contributions

This work was carried out in collaboration among all authors. Author TVD managed the literature searches, performed the statistical analysis and wrote the first draft of the manuscript. Author PDT performed the statistical analysis. Authors TNB, TTH, TCN, DTHH, NTHA, HTS, THL, PQT, NVK, THQ and VVN designed the study and conducted the field works. All authors read and approved the final manuscript.

Article Information

DOI: 10.9734/JPRI/2020/v32i1130551 Editor(s): (1) Dr. Sanjay Nilapwar, Incyte Corporation, USA. Reviewers: (1) Shubhashree, India. (2) Mamdouh Nabi Samy, Minia University, Egypt. Complete Peer review History: http://www.sdiarticle4.com/review-history/58935

Received 01 May 2020 Accepted 07 July 2020 Original Research Article Published 18 July 2020

ABSTRACT

Background: Anoectochilus orchids have been widely used as medicine. However, it has been overharvested in nature because of high commercial values. This study aims at identifying distribution ranges and ecological characteristics of Anoectochilus orchids serving for sustainable development and describing traditional uses by ethnic people in Lai Chau Province, North Vietnam. Methods: Twenty-one plots of 100 m2 each (10 m × 10 m) were established for ecological survey and stand structures were analyzed for vegetation characteristics. While interviewing was applied to gather information on harvesting method, marketing, and medicinal uses. Results: Three Anoectochilus orchids (A. lanceolatus, A. calcareus, and A. setaceus) were found ______

*Corresponding author: E-mail: [email protected];

Bon et al.; JPRI, 32(11): 84-92, 2020; Article no.JPRI.58935

in Lai Chau Province, North Vietnam. These species distribute in both evergreen old-growth and secondary broadleaved forests, and mixed broadleaf-bamboo forest on the elevations of 996–2,134 m. They grow in forests with a high canopy cover of 67 m2 canopy area/ 100 m2 land and high cover (> 90% land) of low vegetation (< 2 m tall). It is believed that using the whole plant of Anoectochilus can treat hypertension and diabetes mellitus and improve the development of underdeveloped children. The folk uses include soaking in alcohol and boiled water for daily drinks like green tea, and consuming as a vegetable. The best harvesting season is during Autumn– Winter and fresh product is mainly marketed with the price of up to 100 U$D/1 kg fresh mass. Conclusion: A. lanceolatus, A. calcareus and A. setaceus are potential forest herbs for poverty reduction to ethnic communities in North Vietnam. The natural populations have been reduced remarkably because of overharvesting. Growing techniques are an urgent need for the conservation and sustainable development of such valuable orchids.

Keywords: Climate condition; elevation zone; folk medicine; herb; poverty reduction.

1. INTRODUCTION pain, stomachache, diabetes, nephritis, high fever, high blood pressure, importance, liver Anoectochilus is a belonging to the family dysfunction, spleen dysfunction, and chest . There are about 50 species throbbing pain [15]. A. setaceus is used for described in genus Anoectochilus. These medicinal oils, treating snakebite poisoning species are known as terrestrial, perennial, [16,17], and A. roxburghii is used to treat , sympodial herbs with a creeping tuberculosis [18]. In addition, Anoectochilus , an upright flowering stem, and dark- leaves are used as vegetables by local colored leaves with contrasting veins [1,2]. The communities and these are also widely flowers are relatively large, hairy and velvety, used for ornamentations because of their and arranged in a short spike. While the fruit is a beautiful leaves and flowers [19]. hairy containing winged seeds [3,4]. The Anoectochilus orchids have natural distributions Anoectochilus orchids have been recorded to from the Himalaya to South , Southeast distribute in high mountainous areas in the Asia, , New Guinea, Melanesia, and Northern provinces of Vietnam [20,21]. It has Hawaii [5]. It is found in evergreen forests with been widely harvested in nature for commercials high moisture and deep shade [1,2]. For example, and therefore contributed significantly to poverty Anoectochilus roxburghii is found in India, reduction to ethnic communities. This has led to Thailand, China, Laos and Vietnam. Its current a remarkable reduction of natural populations. status and medicinal uses were studied in Therefore, understanding the distribution and Darjeeling Himalaya of West Bengal, India [6], ecology of Anoectochilus orchids could support indicating threatened status and value in the development plan and sustainable controlling fever, lung diseases, and management for poverty reduction. This work hypertension. While indiscriminate collection, aims at identifying distribution ranges and deforestation, and extension of agricultural lands ecological characteristics of Anoectochilus are major threats. orchids and describing traditional uses by ethnic people in Lai Chau Province, North Vietnam. Plants of Anoectochilus genus are known as medicinal orchids and have various functions in 2. METHODS traditional medicines such as anti-tumor, lipase decreasing, anti-diabetes, and antihepatitis [7]. 2.1 Study Site The chemical constituents and biological activities of some Anoectochilus herbs were The study was conducted in Lai Chau Province, described [8-11] such as helvolic acid from A. North Vietnam (Fig. 1a; Hoang Sa and Truong setaceus for antibacterial activity [12]. The major Sa Islands of Vietnam are not shown on the chemical components in A. setaceus include α- map). Interviewing responsible persons cadinol, (E,E)-farnesol, and terpinen-4-ol [13]. belonging Provincial Department of Forest While A. formosanus contains β-sitosterol, 4- Development and local citizens was applied to hydroxycinnamic acid, β-D-glucopyranosyloxy, know the potential forests, where Anoectochilus and butanoidglucosides acid [14]. A. formosanus species distribute. The potential areas were first is used to treat many diseases such as chest marked on the maps and then assessed in the

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fields. Old-growth forest (intact and/or less area, crown areas, and low vegetation cover. A disturbed forests) and secondary forest (forests comparison was conducted by univariate recovered after shifting cultivation and/or analysis of variance (ANOVA) using SAS 9.2 at p selective logging) were selected for field data =0.05. collection. 3. RESULTS 2.2 Data Collection

2 3.1 Distribution and Ecology In the field, main plots of 100 m each (10 m × 10 m) were established for data collection. All stems Three Anoectochilus orchids were found in the with a diameter at breast height (DBH) ≥ 5 cm study site, Lai Chau Province, North Vietnam were identified to species, measured for DBH (in (Table 1), including Anoectochilus calcareus, A. cm), height (in meter), and crown diameter (D in c lanceolatus, and A. setaceus (Fig. 1b). In 21 meter). In each main plot, five subplots of 4 m2 survey plots, A. calcareus was found in five plots each (2 m × 2 m) were established in four in old-growth broadleaved forests, A. lanceolatus corners and the middle for a low vegetation was found in four plots in the secondary survey. All vegetation < 2 m tall were recorded in broadleaved forest, and A. setaceus was found these five subplots, including species, height, in 13 plots in both old-growth and secondary density and covering (% of land area). forests of broadleaves and mixed broadleaf-

2.3 Commercial Value and Medicinal Use bamboo (Fig. 1c). A. calcareus and A. lanceolatus were grown together in one plot, Interviewing was applied. The interviewees while in other plots only one species was found. included local ethnic people, Anoectochilus The location with the appearances of these three harvesters, and marketers. Interviewing contents Anoectochilus orchids ranged from 996 m up to included harvesting, marketing and medicinal 2,134 m elevation above sea level. uses. All three Anoectochilus orchids were found in 2.4 Data Analysis evergreen forests of pure broadleaved trees and mixed forest of both broadleaves and bamboo. Characteristics of stand structure were calculated, The forests included both old-growth forest (less including stem density, mean DBH, height, basal disturbed forest) and secondary forest, recovered

Fig. 1. Map of Vietnam and Lai Chau Province (a), three Anoectochilus species in survey areas (b) and forest cover (c)

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after shifting cultivation and/or selective logging. The differences of stand structures in terms of The tree stem densities in these study plots stem density, height and maximum height among ranged 5–12 stems/100 m2, while the range of three orchids were not significantly different species number was 3–12. The forests had a (Table 2). Which were in the range of 7–8 mean DBH of 11.6–42.7 cm, height of 6.8–18.0 stems/100 m2 and canopy height of 9–11 m. m. While the largest stem had DBH of 74.5 cm and a height of 26 m. The total crown area was Structure of crown area distribution in different in the range of 67.5–343.2 m2/100 m2. While in height classes of tree stems was different among low vegetation of shorter than 2 m tall, the stands of three orchids (Fig. 2). A. lanceolatus number of plant clumps was in the range of 5–43 grows in simplest canopy forest, which has only clumps/20 m2, and land covering of low four height classes and less crown area (Fig. 2b) vegetation was in the range of 90–273.3% (Table with the highest crown area in the stems of 9–13 1). m tall. While A. calcareus and A. setaceus grow in forests with more complex canopy, which has There were significant differences of structures five height classes (Fig. 2a, c). Between these (distribution elevation, low vegetation, crown two orchids, there are also differences. The area of canopy trees, mean DBH, and size of highest crown area focused on stems of 14–21 m largest trees) among stands of three orchids tall in A. calcareus (Fig. 2a), while that was in (Table 2). A. setaceus prefers to distribute on the stems of > 17 m tall in A. setaceus, which is lowest elevation of around 1,264 m above sea double that in stems of < 17 m tall (Fig. 2c). level, the distribution elevation (1,777 m) is higher in A. lanceolatus, and the highest 3.2 Commercial Value and Medicinal Use distribution elevation (2,034 m) was found in A. calcareus. Low vegetation significantly affected The price of Anoectochilus orchids is depending the distribution of three orchids as A. setaceus on species. A. lanceolatus costs 0.5 U$D/1 kg distributes in the highest cover of 195% and fresh mass, it is 50 U$D/1 kg fresh mass for A. numerous vegetation clumps of 35/20 m2, calcareus and 100 U$D/1 kg fresh mass for A. reducing to A. lanceolatus with a cover of 153% setaceus. Generally, after harvesting from and 29 clumps/20 m2. While A. calcareus seems natural forests the fresh product is sold at homes to distribute in the lowest vegetation cover of or local markets to outside consumers, who will 150% and vegetation clump of 17/20 m2 (Table resell to trading companies of China mostly. The 2). In addition, A. calcareus grows in the old- best harvesting season is during Autumn-Winter growth forest with the highest difference of stem when Anoectochilus has the highest production sizes including DBH and height. While A. and quality by traditional knowledge. It was lanceolatus grows in secondary forest with much recorded that the availability of Anoectochilus in similar stems sizes. natural forests 10 years ago was numerous

120 120 120 ) ) 2 2 (a) ) (c) 2 m m (b)

m 0 0 0 0 0 90 90 1 0

1 90 / / 1 2 2 / 2 m m ( (

m

( a

a 60 60 e a e 60 r r e a r a

a n

n n w w o w o r

r 30 30

o 30 r C C C

0 0 0 <9 9-13 14-1717-21 >21 <9 9-13 14-1717-21 >21 <9 9-13 14-1717-21 >21 Height class (m) Height class (m) Height class (m)

Fig. 2. Vertical crown structure for A. calcareus stand (a), A. lanceolatus stand (b) and A. setaceus stand (c). Vertical bars indicate +SE

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Table 1. General characteristics of 21 survey plots

Plot ELV Canopy layer (per 100 m2 plot; ±SE) Low vegetation (per 20 m2) Anoectochilus orchids (m) Stems Species DBH DBH max H (m) H max Basal area Crown area Clumps Cover (%) (cm) (cm) (m) (m2) (m2) 1 1,930 10 6 15.5 ±3.2 43.6 8.4 ±0.6 11.0 0.263 139.0 27 156.2 Anoectochilus calcareus 2 2,057 5 4 18.8 ±5.1 29.6 8.9 ±1.7 13.0 0.179 107.0 24 237.8 Anoectochilus calcareus 3 2,123 7 6 25.6 ±6.8 58.3 14.0 ±2.4 24.0 0.513 146.1 5 100.0 Anoectochilus calcareus 4 2,134 6 6 42.7 ±8.7 74.5 18.0 ±1.7 24.0 1.038 175.9 15 141.5 Anoectochilus calcareus 5 1,930 9 8 17.2 ±2.5 27.7 9.7 ±0.7 12.0 0.243 168.9 14 119.0 A. calcareus and A. lanceolatus 6 1,906 5 4 15.5 ±2.0 20.4 8.8 ±1.0 12.0 0.100 67.5 23 99.9 Anoectochilus lanceolatus 7 1,894 7 4 13.4 ±2.3 23.2 8.1 ±1.2 14.0 0.116 97.4 19 131.7 Anoectochilus lanceolatus 8 1,915 8 8 16.2 ±2.2 26.9 10.9 ±1.0 17.0 0.185 134.5 27 198.9 Anoectochilus lanceolatus 9 1,395 12 10 11.6 ±1.3 23.6 8.7 ±0.8 14.0 0.143 134.3 51 184.6 10 1,434 12 9 14.3 ±1.5 24.8 9.3 ±0.7 13.0 0.216 106.8 26 244.0 Anoectochilus setaceus 11 1,009 7 3 19.9 ±2.3 26.1 12.6 ±0.6 14.0 0.234 166.5 38 174.4 Anoectochilus setaceus 12 996 6 5 14.4 ±3.5 26.4 9.8 ±1.6 15.0 0.127 106.0 30 272.5 Anoectochilus setaceus 13 1,010 6 6 18.5 ±3.6 29.0 10.3 ±1.3 14.0 0.191 81.7 37 136.1 Anoectochilus setaceus 14 1,192 8 4 16.6 ±2.4 24.5 9.8 ±0.9 13.0 0.200 125.7 35 209.5 Anoectochilus setaceus 15 1,220 8 6 18.7 ±4.7 39.5 11.2 ±1.8 19.0 0.318 168.1 39 273.3 Anoectochilus setaceus 16 1,208 7 7 14.4 ±3.3 30.9 9.9 ±1.4 16.0 0.149 84.0 35 222.1 Anoectochilus setaceus 17 1,229 9 8 17.0 ±2.8 29.9 11.1 ±1.3 17.0 0.248 118.6 38 219.8 Anoectochilus setaceus 18 1,472 7 7 13.4 ±3.0 24.8 6.8 ±0.6 8.5 0.128 48.7 38 90.0 Anoectochilus setaceus 19 1,472 8 7 11.6 ±1.2 16.2 8.4 ±0.8 12.0 0.090 74.6 35 138.5 Anoectochilus setaceus 20 1,459 7 6 10.1 ±0.9 12.7 8.3 ±0.9 11.0 0.059 63.6 32 126.1 Anoectochilus setaceus 21 1,473 7 7 35.2 ±7.0 65.9 17.0 ±2.1 26.0 0.842 343.2 43 236.7 Anoectochilus setaceus ELV is elevation above sea level

Table 2. Comparisons of stand structures (±SE) among three Anoectochilus orchids

Canopy layer (per 100 m2 plot) Low vegetation (per 20 m2) ELV (m) Anoectochilus orchids 2 Stems DBH (cm) DBHmax (cm) H (m) Hmax (m) Crown area (m ) Clump Cover (%) 7.4 ±0.9 23.9a ±5.0 46.7a ±8.9 11.8 ±1.8 16.8 ±3.0 147.4a ±12.2 17.0a ±3.9 150.9a ±23.7 2,034a ±44.8 A. calcareus 8.0 ±1.5 14.2b ±1.0 23.5b ±1.3 9.1 ±0.6 14.2 ±1.0 108.4b ±16.2 29.9ab ±7.2 153.7a ±23.1 1,777b ±127.6 A. lanceolatus 7.6 ±0.5 17.0c ±1.9 29.2c ±3.9 10.3 ±0.7 14.8 ±1.3 123.9ab ±22.6 35.5b ±1.3 195.2b ±17.6 1,264c ±55.7 A. setaceus Different letters a, b, c in a indicate significant difference of means at p =0.05. ELV is the elevation above sea level

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which can be easily found at any old-growth disturbance, while still keeps suitable canopy forest. Recently, it is difficult to find out cover. The plants were only found near water Anoectochilus even in remote old-growth forests. bodies, growing on soil with a high humus layer A person takes one day to harvest 0.2 kg fresh and high humidity, indicating the importance of mass of Anoectochilus nowadays, compared to humidity on the distribution and growth of A. several kilograms in the past ten years. Around lanceolatus. 80% harvest product is marketed and the rest is used by local people. Anoectochilus calcareus Aver is native species of Vietnam and found in evergreen coniferous and In the study site, the whole plant of broadleaved forests on rocky limestone in Anoectochilus is used to treat hypertension and northern Vietnam on the elevations of 450–1,600 diabetes mellitus. Underdeveloped children can m [27]. In the present study, the species was use this to improve appetite and support found in North Vietnam (22°08’20.1’’N and digestion. Folk uses include soaking in alcohol 103°54’34.3’’E) on the elevation of 1,930–2,134 for daily drinks and soaking in boiled water like m in the old-growth evergreen broadleaved forest. green tea, or consuming as vegetables. The elevation range is higher than previously reported, indicating a wider distribution range of 4. DISCUSSION A. calcareus. In addition, it was found growing on soil other than rocky limestone previously 4.1 Distribution and Ecology reported [27]. This again indicates the wider ecological conditions for distribution and growth Anoectochilus species are terrestrial plants, of A. calcareus, and therefore it could be found to growing in soil, leaf litter, humus, and also on have natural distributions further to southern mossy rocks in lowland and mid-mountain forests Vietnam. up to 2,135 m elevation [6,22]. Like other forest herbs [23,24], Anoectochilus is shade-tolerant Anoectochilus setaceus Blume is found in China, plants (Fig. 1 b, c), which can only survive and India, Bangladesh, Nepal, , Sri Lanka, grow under shade. The shading level is different Myanmar, Thailand, Vietnam and Indonesia. The among Anoectochilus species [25]. This was species grows in evergreen broadleaved forests confirmed in the present study as the differences on the elevations of 1,200–1,800 m [28,29]. In of stand structures among three Anoectochilus the present study, it was found in North Vietnam species, especially in terms of low vegetation (22°44’35.4’’N and 103°24’56.7’’E) on the and crown area (Table 2; Fig. 2). In addition, in elevation of 996–1,473 m in both old-growth and 20 of 21 plots surveyed only single Anoectochilus secondary evergreen broadleaved forests and orchid was found in a plot. This indicated the mixed broadleaf-bamboo forest in all foot, middle difference in ecology requirements among three and top of the mountains. The lower elevation orchids. Therefore, it is difficult for these orchids distribution found in the present study indicates to grow in the same vegetation. The many the wider distribution of A. setaceus. In addition, differences of vertical crown structures among it can grow in several types of vegetation which three orchids (Fig. 2) indicate the difference of have high shading levels and in all mountain light regime penetrating to the forest floor, which positions. Therefore, ecological conditions for A. plays an important role in survival and growth of setaceus are quite wide. But the most important forest herbs. condition is the vegetation cover. It should be high enough to ensure shading for this orchid Anoectochilus lanceolatus Lindl is found in the (Table 2; Fig. 2c). Himalayas, Nepal, Bangladesh, Myanmar, Taiwan, Thailand, and Vietnam [5]. It grows on The natural populations of Anoectochilus are shaded rocks in deep shade broadleaved forests under threat from overharvest, habitat reduction, on elevations of 800–2,200 m [26]. In the present and forest fragmentation [6,7,19,30]. Therefore, study, the species was found in North Vietnam in each region and country where such plants are (22°07’43.3’’N and 103°54’44.2’’E) on the now available [6], preservation plan should be elevation of 1,894–1,915 m close to streams with established for successful protection and future high humidity. The species was found in both development. The commercial price of these secondary and old-growth evergreen three Anoectochilus orchids is much different. broadleaved forest. It grows in deep shade This is believed to relate to the medicinal values evergreen broadleaved forest but even can grow of compounds in each species. Therefore, further in secondary forest with some levels of human studies on medicinal compounds must be

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conducted for further recommendations on Anoectochilus orchids in North Vietnam conservation, usage and development. sustainably.

4.2 Commercial Value and Medicinal Use CONSENT

Anoectochilus species have been widely used as It is not applicable. folk medicine in China, Sri Lanka, Taiwan, and Vietnam for centuries [22,31,32]. It is used E T H I C A L A PPROVAL to treat cancer, hypertension, diabetes mellitus, lung and liver diseases, nephritis, impotence, It is not applicable. spleen disorder, pleurodynia, and underdeveloped children [33-35]. Therefore, currently, it has been widely used in modern ACKNOWLEDGEMENT medicines. For example, quercetin‐7‐O‐β‐D ‐[6”‐O‐(trans‐feruloyl)]‐glucopyranoside This research is funded by the Lai Chau compound isolated from an extract of A. Department of Science and Technology. We roxburghii exhibits strong scavenging activity would like to thank anonymous reviewers for against the 1,1‐diphenyl‐2‐picrylhydrazyl free constructive comments on the manuscript. radical [36]. Anoectochilus orchids could be considered as potential plants for both folk and COMPETING INTERESTS modern medicines recently and in the future. Authors have declared that no competing With a high price of up to 100 U$D/1 kg fresh interests exist. mass of A. setaceus in Vietnam recently, it is a potential forest herb for poverty reduction. As the REFERENCES local community in mountainous areas is living in a much lower standard compared to other parts 1. Jones DL. A complete guide to native of Vietnam. However, growing Anoectochilus is orchids of Australia including the island not easy work and the plants grow quite slow. territories. Frenchs Forest, NSW, New Growing Anoectochilus orchids in local Holland. 2006;346. communities for production purposes is not 2. Anoectochilus. Australian National Botanic available other than for ornamentation. Therefore, Gardens; 2020. researching for simple and applicable growing (Retrieved on 16 June 2020) techniques for Anoectochilus orchids should be 3. Anoectochilus. Flora of China; 2020. conducted and the best one must be (Retrieved on 16 June 2020) recommended for practical application. 4. Genus: Anoectochilus. North American Orchid Conservation Center; 2020. 5. CONCLUSION (Retrieved on 16 June 2020) 5. Kew World Checklist of selected plant Anoectochilus lanceolatus, A. calcareus, and A. families; 2020. setaceus are three orchids found in Lai Chau (Retrieved on 16 June 2020) Province, North Vietnam. These species 6. Yonzone R. Current availability status and distribute in evergreen old-growth and secondary medicinal uses of Anoectochilus roxburghii broadleaved forests, and mixed broadleaf- (Wall.) Lindl. (Orchidaceae) in Darjeeling bamboo forest on the elevations of 996–2,134 m Himalaya of West Bengal, India. Trends in above sea level. These orchids are used locally Biosciences. 2017;10:6565-6568. by soaking in alcohol and boiled water for daily 7. Thuy TTH, Gam DT, Hung NK, Ngoc P, Ha drinks like green tea, and consuming as HC. In vitro micropropagation of an vegetables. This is believed to have positive endangered medicinal orchild impacts on hypertension, diabetes mellitus and (Anoectochilus setaceus Blume) through underdeveloped children. Such high medical protocorm-like bodies. Vietnam Ecology values have led to remarkably reduced Journal. 2015;37:76-83. populations of Anoectochilus orchids in nature. 8. Cai J, Zhao, Zhu E. A new flavonol Therefore, researches on growing, harvesting, triglycoside derived from Anoectochilus and processing are an urgent need, which can elwesii on stimulating glucose uptake in contribute to preserving and developing insulin-induced human HepG2 cells.

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